Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus

Cytoplasmic male sterility (CMS) lines are widely used for hybrid production in Brassica napus. The Shaan2A CMS system is one of the most important in China and has been used for decades; however, the male sterility mechanism underlying Shaan2A CMS remains unknown. Here, we performed transcriptomic...

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Main Authors: Luyun Ning, Hao Wang, Dianrong Li, Zhiwei Lin, Yonghong Li, Weiguo Zhao, Hongbo Chao, Liyun Miao, Maoteng Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00252/full
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spelling doaj-61bf7bcaf7204f369438de839a4be5752020-11-25T01:10:17ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-03-011010.3389/fpls.2019.00252440621Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napusLuyun Ning0Hao Wang1Dianrong Li2Zhiwei Lin3Yonghong Li4Weiguo Zhao5Weiguo Zhao6Hongbo Chao7Liyun Miao8Maoteng Li9Maoteng Li10Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaHybrid Rape Research Center of Shaanxi Province, Shaanxi Rapeseed Branch of National Centre for Oil Crops Genetic Improvement, Yangling, ChinaHybrid Rape Research Center of Shaanxi Province, Shaanxi Rapeseed Branch of National Centre for Oil Crops Genetic Improvement, Yangling, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaHybrid Rape Research Center of Shaanxi Province, Shaanxi Rapeseed Branch of National Centre for Oil Crops Genetic Improvement, Yangling, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaHybrid Rape Research Center of Shaanxi Province, Shaanxi Rapeseed Branch of National Centre for Oil Crops Genetic Improvement, Yangling, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaHubei Collaborative Innovation Center for the Characteristic Resources Exploitation of Dabie Mountains, Huanggang Normal University, Huanggang, ChinaCytoplasmic male sterility (CMS) lines are widely used for hybrid production in Brassica napus. The Shaan2A CMS system is one of the most important in China and has been used for decades; however, the male sterility mechanism underlying Shaan2A CMS remains unknown. Here, we performed transcriptomic and proteomic analysis, combined with additional morphological observation, in the Shaan2A CMS. Sporogenous cells, endothecium, middle layer, and tapetum could not be clearly distinguished in Shaan2A anthers. Furthermore, Shaan2A anther chloroplasts contained fewer starch grains than those in Shaan2B (a near-isogenic line of Shaan2A), and the lamella structure of chloroplasts in Shaan2A anther wall cells was obviously aberrant. Transcriptomic analysis revealed differentially expressed genes (DEGs) mainly related to carbon metabolism, lipid and flavonoid metabolism, and the mitochondrial electron transport/ATP synthesis pathway. Proteomic results showed that differentially expressed proteins were mainly associated with carbohydrate metabolism, energy metabolism, and genetic information processing pathways. Importantly, nine gene ontology categories associated with anther and pollen development were enriched among down-regulated DEGs at the young bud (YB) stage, including microsporogenesis, sporopollenin biosynthetic process, and tapetal layer development. Additionally, 464 down-regulated transcription factor (TF) genes were identified at the YB stage, including some related to early anther differentiation such as SPOROCYTELESS (SPL, also named NOZZLE, NZZ), DYSFUNCTIONAL TAPETUM 1 (DYT1), MYB80 (formerly named MYB103), and ABORTED MICROSPORES (AMS). These results suggested that the sterility gene in the Shaan2A mitochondrion might suppress expression of these TF genes in the nucleus, affecting early anther development. Finally, we constructed an interaction network of candidate proteins based on integrative analysis. The present study provides new insights into the molecular mechanism of Shaan2A CMS in B. napus.https://www.frontiersin.org/article/10.3389/fpls.2019.00252/fullcytoplasmic male sterilitytranscriptomeproteometranscription factoranther differentiationmitochondria
collection DOAJ
language English
format Article
sources DOAJ
author Luyun Ning
Hao Wang
Dianrong Li
Zhiwei Lin
Yonghong Li
Weiguo Zhao
Weiguo Zhao
Hongbo Chao
Liyun Miao
Maoteng Li
Maoteng Li
spellingShingle Luyun Ning
Hao Wang
Dianrong Li
Zhiwei Lin
Yonghong Li
Weiguo Zhao
Weiguo Zhao
Hongbo Chao
Liyun Miao
Maoteng Li
Maoteng Li
Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
Frontiers in Plant Science
cytoplasmic male sterility
transcriptome
proteome
transcription factor
anther differentiation
mitochondria
author_facet Luyun Ning
Hao Wang
Dianrong Li
Zhiwei Lin
Yonghong Li
Weiguo Zhao
Weiguo Zhao
Hongbo Chao
Liyun Miao
Maoteng Li
Maoteng Li
author_sort Luyun Ning
title Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
title_short Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
title_full Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
title_fullStr Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
title_full_unstemmed Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus
title_sort transcriptomic and proteomic analysis of shaan2a cytoplasmic male sterility and its maintainer line in brassica napus
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-03-01
description Cytoplasmic male sterility (CMS) lines are widely used for hybrid production in Brassica napus. The Shaan2A CMS system is one of the most important in China and has been used for decades; however, the male sterility mechanism underlying Shaan2A CMS remains unknown. Here, we performed transcriptomic and proteomic analysis, combined with additional morphological observation, in the Shaan2A CMS. Sporogenous cells, endothecium, middle layer, and tapetum could not be clearly distinguished in Shaan2A anthers. Furthermore, Shaan2A anther chloroplasts contained fewer starch grains than those in Shaan2B (a near-isogenic line of Shaan2A), and the lamella structure of chloroplasts in Shaan2A anther wall cells was obviously aberrant. Transcriptomic analysis revealed differentially expressed genes (DEGs) mainly related to carbon metabolism, lipid and flavonoid metabolism, and the mitochondrial electron transport/ATP synthesis pathway. Proteomic results showed that differentially expressed proteins were mainly associated with carbohydrate metabolism, energy metabolism, and genetic information processing pathways. Importantly, nine gene ontology categories associated with anther and pollen development were enriched among down-regulated DEGs at the young bud (YB) stage, including microsporogenesis, sporopollenin biosynthetic process, and tapetal layer development. Additionally, 464 down-regulated transcription factor (TF) genes were identified at the YB stage, including some related to early anther differentiation such as SPOROCYTELESS (SPL, also named NOZZLE, NZZ), DYSFUNCTIONAL TAPETUM 1 (DYT1), MYB80 (formerly named MYB103), and ABORTED MICROSPORES (AMS). These results suggested that the sterility gene in the Shaan2A mitochondrion might suppress expression of these TF genes in the nucleus, affecting early anther development. Finally, we constructed an interaction network of candidate proteins based on integrative analysis. The present study provides new insights into the molecular mechanism of Shaan2A CMS in B. napus.
topic cytoplasmic male sterility
transcriptome
proteome
transcription factor
anther differentiation
mitochondria
url https://www.frontiersin.org/article/10.3389/fpls.2019.00252/full
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